Technical Abstract:
Mycotoxins, and especially the aflatoxins, are an enormous problem in agriculture, with aflatoxin B1 being the most carcinogenic known natural compound. The worldwide costs associated with aflatoxin monitoring and crop losses are in the hundreds of millions of dollars. Aspergillus flavus and A. parasiticus are the most common agents of aflatoxin contamination of oil-rich seed and grain crops. Sexually compatible strains vary greatly in their degree of fertility. Differences in fertility may be the result of female sterility, changes in DNA methylation, epistatic interactions between genetically different nuclei or other epigenetic modifications. We are currently exploring these possibilities using sexual crosses. The extent to which sexual and asexual reproduction restricts genetic exchange and recombination in these species is largely unknown, but is critical to understand for both fundamental and practical applications, such as biological control. To study this we examined natural genetic variation in A. flavus and A. parasiticus sampled from single peanut fields in the United States, Africa, Argentina, Australia and India. We found that differences in the proportions of MAT1-1 and MAT1-2 were correlated with the amount of asexual and sexual reproduction in populations. For both A. flavus and A. parasiticus, when the number of MAT1-1 and MAT1-2 was significantly different, there was extensive linkage disequilibrium in the aflatoxin cluster and isolates grouped into specific toxin classes, either the non-aflatoxigenic class in A. flavus or the B1-dominant and G1-dominant classes in A. parasiticus. We compared these results to variation in experimental populations. Crossovers in the aflatoxin cluster of F1 progeny coincided with recombination hotspots observed in natural populations, indicating that a single generation of sex can generate contemporary patterns of recombination and toxin diversity. Our work shows that a combination of ecological factors, asexual/sexual reproduction and balancing selection may influence aflatoxin diversity in these agriculturally important fungi.